Skip to main content

Advertisement

Log in

Redox balance and mitochondrial glycerol phosphate dehydrogenase activity in trained rats

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Free radical production is increased in many disease states and during exercise, but in the latter the concurrent stimulation of the antioxidant defense system seems to protect the organism from excessive production of reactive oxygen species. Chronic exercise can exert negative effects on the activity of mitochondrial glycerol phosphate dehydrogenase (mGPdH), which may offer some explanation for the antioxidant effects of training, since this enzyme is a relevant producer of free radicals. To test this correlation, we compared mGPdH activity, two antioxidant defense markers and two markers of oxidative stress in sedentary and trained (Tr) rats. Training was through a swimming exercise 3 days a week. After 8 weeks, Tr rats lasted twice as long as controls in an acute swimming test with a 5% load. Forty-eight hours after the last exercise, the animals were killed to collect blood and tissues. Tr animals presented lower body weight and visceral fat mass with lower triglyceride content in visceral fat and plasma (p < 0.05). The specific activity of mGPdH in muscle mitochondria was reduced in Tr rats by 88% (p < 0.05). Total antioxidant capacity, lipid peroxidation and reduced glutathione (GSH) in liver and muscle were unaltered, while plasma GSH increased by 21% (p < 0.05). These data suggest a profile of successful redox equilibrium maintenance in Tr rats, with a potentially significant contribution from the lower level of mGPdH activity in muscle. This training protocol appears to be suitable for use in detailed studies of biochemical adaptations to oxidative stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Adhihetty PJ, Ljubicic V, Menzies KJ, Hood DA (2005) Differential susceptibility of subsarcolemmal and intermyofibrillar mitochondria to apoptotic stimuli. Am J Cell Physiol 289:C994–C1001

    Article  CAS  Google Scholar 

  • Amler E, Rauchová H, Svobododá J, Drahota Z (1986) Regulation of glycerol 3-phosphate oxidation in mitochondria by changes in membrane microviscosity. FEBS J 206:1–3

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Brand MD (2010) The sites and topology of mitochondrial superoxide production. Exp Gerontol 45:466–472

    Article  PubMed  CAS  Google Scholar 

  • Bray GA, Mothon S, Cohen A (1969) Effect of diet and triidothyronine on the activity of sn-glycerol-3-phosphate dehydrogenase and on the metabolism of glucose and pyruvate by adipose tissue of obese patients. J Clin Invest 48:1413–1422

    Article  PubMed  CAS  Google Scholar 

  • Burgomaster KA, Heigenhauser GJF, Gibala MJ (2006) Effect of short-term sprint interval training on human skeletal muscle carbohydrate metabolism during exercise and time trial performance. J Appl Physiol 100:2041–2047

    Article  PubMed  Google Scholar 

  • Casimiro-Lopes G, Alves SB, Salerno VP, Passos MC, Lisboa PC, Moura EG (2008) Maximum acute exercise tolerance in hyperthyroid and hypothyroid rats subjected to forced swimming. Horm Metab Res 40:276–280

    Article  PubMed  CAS  Google Scholar 

  • Chowdhury SKR, Gemin A, Singh G (2005) High activity of mitochondrial glycerophosphate dehydrogenase and glycerophosphate-dependent ROS production in prostate cell cancer lines. Biochem Biophys Res Commun 333:1139–1145

    Article  PubMed  CAS  Google Scholar 

  • Drahota Z, Chowdhury SK, Floryk D, Mrácek T, Wilhelm J, Rauchová H, Lenaz G, Houstek J (2002) Glycerophosphate-dependent hydrogen peroxide production by brown adipose tissue mitochondria and its activation by ferricyanide. J Bioenerg Biomembr 34:105–113

    Article  PubMed  CAS  Google Scholar 

  • Essén-Gustafsson B, Tesch PA (1990) Glycogen and triglyceride utilization in relation to muscle metabolic characteristics in men performing heavy-resistance exercise. Eur J Appl Physiol 61:5–10

    Article  Google Scholar 

  • Folch J, Lees M, Sloane-Standley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Fried GH, Greenberg N, Antopol W (1961) Determination of alpha-glycerophosphate oxidation with tetrazolium. Proc Soc Exp Biol 107:523–631

    PubMed  CAS  Google Scholar 

  • Fujimoto E, Machida S, Higuchi M, Tabata I (2010) Effects of nonexhaustive bouts of high-intensity intermittent swimming training on GLUT-4 expression in rat skeletal muscle. J Physiol Sci 60:95–101

    Article  PubMed  CAS  Google Scholar 

  • Guo Z, Jensen MD (1999) Blood glycerol is an important precursor for intramuscular triacylglycerol synthesis. J Biol Chem 274:23702–23706

    Article  PubMed  CAS  Google Scholar 

  • Horowitz JF (2003) Fatty acid mobilization from adipose tissue during exercise. Trends Endocrinol Metab 14:386–392

    Article  PubMed  CAS  Google Scholar 

  • Hurley BF, Nemeth PM, Martin WH III, Hagberg JM, Dalsky GP, Holloszy JO (1986) Muscle triglyceride utilization during exercise: effect of training. J Appl Physiol 60:562–567

    PubMed  CAS  Google Scholar 

  • Janaszewska A, Bartosz G (2002) Assay of total antioxidant capacity: a comparison of four methods as applied to human blood plasma. Scand J Clin Lab Invest 62:231–236

    Article  PubMed  CAS  Google Scholar 

  • Jensen MD (2002) Fatty acid oxidation in human skeletal muscle. J Clin Invest 110:1607–1609

    PubMed  CAS  Google Scholar 

  • Krieger DA, Tate CA, McMillin-Wood J, Booth FW (1980) Populations of rat skeletal muscle mitochondria after exercise and immobilization. J Appl Physiol Respir Env Exer Physiol 48:23–28

    CAS  Google Scholar 

  • Lanza IR, Nair KS (2009) Functional assessment of isolated mitochondria in vitro. Meth Enzymol 457:349–372

    Article  PubMed  CAS  Google Scholar 

  • Lee Y, Lardy HA (1965) Influence of thyroid hormones on l-alpha-glycerophosphate dehydrogenases and other dehydrogenases in various organs of the rat. J Biol Chem 240:1427–1436

    PubMed  CAS  Google Scholar 

  • Leeuwenburgh C, Ji LL (1995) Glutathione depletion in rested and exercised mice: biochemical consequence and adaptation. Arch Biochem Biophys 316:941–947

    Article  PubMed  CAS  Google Scholar 

  • Look MP, Rockstroh JK, Rao GS, Kreuzer KA, Barton S, Lemoch H, Sudhop T, Hoch J, Stockinger K, Spengler U, Sauerbruch T (1997) Serum selenium, plasma glutathione (GSH) and erythrocyte glutathione peroxidase (GSH-Px)-levels in asymptomatic versus symptomatic human immunodeficiency virus-1 (HIV-1)-infection. Eur J Clin Nutr 51:266–272

    Article  PubMed  CAS  Google Scholar 

  • Lu S (1999) Regulation of hepatic glutathione synthesis: current concepts and controversies. FASEB J 13:1169–1183

    PubMed  CAS  Google Scholar 

  • MacDonald MJ (1981) High contend of mitochondrial glycerol-3-phosphate dehydrogenase in pancreatic islets and its inhibition by diazoxide. J Biol Chem 256:8287–8290

    PubMed  CAS  Google Scholar 

  • MacDonald MJ, Brown LJ (1996) Calcium activation of mitochondrial glycerol phosphate dehydrogenase restudied. Arch Biochem Biophys 326:79–84

    Article  PubMed  CAS  Google Scholar 

  • Margonis K, Fatouros IG, Jamurtas A, Nikolaidis MG, Douroudos I, Chatzinikolaou A, Mitrakou A, Mastorakos G, Papassotiriou I, Taxildaris K, Kouretas D (2007) Oxidative biomarkers responses to physical overtraining: implications for diagnosis. Free Rad Biol Med 43:901–910

    Article  PubMed  CAS  Google Scholar 

  • McGowan MW, Artiss JD, Strandbergh DR, Zak B (1983) A peroxidase-coupled method for the colorimetric determination of serum triglycerides. Clin Chem 29:538–542

    PubMed  CAS  Google Scholar 

  • Melanson EL, Maclean PS, Hill JO (2009) Exercise improves fat metabolism in muscle but does not increase 24-h fat oxidation. Exerc Sport Sci Rev 37:93–101

    Article  PubMed  Google Scholar 

  • Oberbach A, Bossenz Y, Lehmann S, Niebauer J, Adams V, Paschke R, Schön MR, Blüher M, Punkt K (2006) Altered fiber distribution and fiber specific glycolytic and oxidative enzyme activity in skeletal muscle of diabetic patients with type 2 diabetes. Diabetes Care 29:895–900

    Article  PubMed  CAS  Google Scholar 

  • Ohta A, Mohri T, Ohyashiki T (1989) Effect of lipid peroxidation on membrane-bound Ca2+-ATPase activity of the intestinal brush-border membranes. Biochim Biophys Acta 984:151–157

    Article  PubMed  CAS  Google Scholar 

  • Palmer JW, Tandler B, Hoppel C (1977) Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle. J Biol Chem 252:8731–8739

    PubMed  CAS  Google Scholar 

  • Palmer JW, Tandler B, Hoppel C (1985) Biochemical differences between subsarcolemmal and interfibrillar mitochondria from rat cardiac muscle: effects of procedural manipulations. Arch Biochem Biophys 236:691–702

    Article  PubMed  CAS  Google Scholar 

  • Pinho RA, Andrades ME, Oliveira MR, Pirola AC, Zago MS, Silveira PCL, Dal-Pizzol F, Moreira JCF (2006) Imbalance in SOD/CAT activities in rat skeletal muscles submitted to treadmill training exercise. Cell Biol Int 30:848–853

    Article  PubMed  CAS  Google Scholar 

  • Pradhan D, Weiser M, Lunley-Sapanski K, Frazier D, Williamson P, Schlegel RA (1990) Peroxidation-induced perturbations of erythrocyte lipid organization. Biochim Biophys Acta 1023:398–404

    Article  PubMed  CAS  Google Scholar 

  • Praet SFE, van Loon LJC (2009) Exercise therapy in Type 2 diabetes. Acta Diabetol 46:263–278

    Article  PubMed  Google Scholar 

  • Qiao D, Hou L, Liu X (2006) Influence of intermittent anaerobic exercise on mouse physical endurance and antioxidant components. Br J Sports Med 40:214–218

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen UF, Krustrup P, Bangsbo J, Rasmussen HN (2001) The effect of high-intensity exhaustive exercise studied in isolated mitochondria from human skeletal muscle. Pflügers Arch 443:180–187

    Article  PubMed  CAS  Google Scholar 

  • Rauchová H, Drahota Z, Rauch P, Fato R, Lenaz G (2003) Coenzyme Q releases the inhibitory effect of free fatty acids on mitochondrial glycerophosphate dehydrogenase. Acta Biochim Pol 50:405–413

    PubMed  Google Scholar 

  • Rauchová H, Vrbacky M, Bergamini C, Fato R, Lenaz G, Houstek J, Drahota Z (2006) Inhibition of glycerophosphate-dependent H2O2 generation in brown fat mitochondria by idebenone. Biochem Biophys Res Commun 339:362–366

    Article  PubMed  Google Scholar 

  • Sacktor R, Wormser-Shavit E, Whiite JI (1965) Diphosphopyridine nucleotide-linked cytoplasmic metabolites in rat leg muscle in situ during contraction and recovery. J Biol Chem 240:2678–2681

    PubMed  CAS  Google Scholar 

  • Senturk UK, Gundu F, Kuru O, Aktekin MR, Kipmen D, Yalçcin O, Bor-Küçükatay M, Yesilkaya A, Baskurt OK (2001) Exercise-induced oxidative stress affects erythrocytes in sedentary rats but not exercise-trained rats. J Appl Physiol 91:1999–2004

    PubMed  CAS  Google Scholar 

  • Simões HG, Campbell CSG, Kokubun E, Denadai BS, Baldissera V (1990) Blood glucose responses in humans mirror lactate responses for individual anaerobic threshold and for lactate minimum in track tests. Eur J Appl Physiol 80:34–40

    Article  Google Scholar 

  • Tabata I, Nishimura K, Kouzaki M, Hirai Y, Ogita F, Miyachi M, Yamamoto K (1996) Effects of moderate-intensity endurance and high-intensity intermittent training on anaerobic capacity and VO2max. Mec Sci Sports Exerc 28:1327–1330

    Article  CAS  Google Scholar 

  • Terada S, Yokozek T, Kawanaka K, Ogawa K, Higuchi M, Ezaki O, Tabata T (2001) Effects of high-intensity swimming training on GLUT-4 and glucose transport activity in rat skeletal muscle. J Appl Physiol 90:2019–2024

    PubMed  CAS  Google Scholar 

  • Terada S, Tabata I, Higuchi M (2004) Effects of high-intensity swimming training on fatty acid oxidation enzyme activity in rat skeletal muscle. Jpn J Physiol 54:47–52

    Article  PubMed  CAS  Google Scholar 

  • Terada S, Kawanaka K, Goto M, Shimokawa T, Tabata I (2005) Effects of high-intensity intermittent swimming on PGC-1a protein expression in rat skeletal muscle. Acta Physiol Scand 184:59–65

    Article  PubMed  CAS  Google Scholar 

  • Tretter L, Takacs K, Hegedus V, Adam-Vizi V (2007) Characteristics of α-glycerophosphate evoked H2O2 generation in brain mitochondria. J Neurochem 100:650–663

    Article  PubMed  CAS  Google Scholar 

  • van Hall G, Sacchetti M, Rådegran G, Saltin B (2002) Human skeletal muscle fatty acid and glycerol metabolism during rest, exercise and recovery. J Physiol 543:1047–1058

    Article  PubMed  Google Scholar 

  • Watkins PJ (2003) Cardiovascular disease, hypertension, and lipids. Br Med J 326:874–876

    Article  Google Scholar 

  • Zambon AC, McDearmon EL, Salomonis N, Vranizan KM, Johansen KL, Adey D, Takahashi JS, Schambelan M, Conklin BR (2003) Time- and exercise-dependent gene regulation in human skeletal muscle. Genome Biol 4:1–12

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ). We are grateful to Dr. Antonio Galina (Instituto de Bioquímica Médica) for helpful discussions.

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Verônica P. Salerno.

Additional information

Communicated by Susan A. Ward.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casimiro-Lopes, G., Ramos, D., Sorenson, M.M. et al. Redox balance and mitochondrial glycerol phosphate dehydrogenase activity in trained rats. Eur J Appl Physiol 112, 3839–3846 (2012). https://doi.org/10.1007/s00421-012-2368-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-012-2368-y

Keywords

Navigation